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Transcriptional Regulation in Plants: the Importance of Combinatorial Control

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Transcriptional Regulation in Plants: the Importance of Combinatorial Control Plant Physiol. (1998) 118: 1111–1120 Update on Gene Regulation Transcriptional Regulation in Plants: The Importance of Combinatorial Control Karam B. Singh Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, California 90095–1606 GLOSSARY OF TERMS plant-defense/stress response. A major level at which gene expression is regulated is the initiation of transcription, Combinatorial control: use of a discrete number of tran- and this is reflected in the percentage of the genome ded- scription factors in different combinations to give rise to icated to transcription factors in plants and other eu- a wide spectrum of expression patterns. karyotes. For example, an analysis of 1.9 Mb of Arabidopsis Enhanceosome: a higher-order nucleoprotein complex that genomic sequence from chromosome 4 revealed that about is formed by the binding of a specific combination of 15% of the genes with predicted or known functions were transcription factors to the transcriptional regulatory se- involved in transcription, a percentage similar to what has quences of a particular gene. been found in other eukaryotes (Bevan et al., 1998). General transcription factors: components of the Pol II In eukaryotic cells, genomic DNA is complexed with transcription-initiation complex that are thought to be proteins to form chromatin. One of chromatin’s major roles common to all Pol II promoters. is to facilitate the packaging of DNA in the nucleus, but the Holoenzyme: a large protein complex that is preformed structure of chromatin also leads to a general suppression off of the DNA and contains Pol II and many of the of gene activity. For gene activation and transcription to other components of the Pol II transcription-initiation occur, the chromatin in the vicinity of the gene must be complex. remodeled to allow access for transcription factors and Pol II transcription-initiation complex: a large protein ma- the recruitment of the RNA polymerase II (Pol II) chine that contains dozens of polypeptides and assem- transcription-initiation complex. Transcription factors play bles near the transcription start site. important and diverse roles in gene expression, including Transcriptional activators: class of regulatory proteins that chromatin remodeling and recruitment/stabilization of the are gene specific and function to increase transcription Pol II transcription-initiation complex. Transcription fac- from target promoters. tors, which come in many shapes and sizes, can be divided Transcriptional synergy: when specific combinations of into a number of functional classes, with some proteins transcription factors give rise to significantly higher lev- els of transcription than the sum of the additive effects belonging to more than one class. A major class of tran- obtained when each factor is assayed individually. scription factors is activators and repressors. These pro- teins bind to specific DNA sequences found only in certain During their development and differentiation, plants promoters and are instrumental in giving rise to gene- need to integrate a wide range of tissue, developmental, specific regulation. A second class of transcription factors and environmental signals to regulate complex patterns of are coactivators or corepressors. These proteins mediate gene expression. The regulation of seed-storage protein the transcriptional effects of specific activators/repressors, gene expression, resulting in expression during specific in some cases by remodeling chromatin. Whereas this stages of seed development but not in other parts of the group of transcription factors are typically not able to bind plant, is a striking example of tissue and developmental to DNA on their own, they can still be promoter-specific as control and is of considerable agricultural importance. a result of protein-protein interactions with specific activa- Plants also have unique needs and strategies for respond- tors and repressors. A third class comprises the general ing to changes in their environment. When light strikes an transcription factors, which are important components of etiolated leaf, numerous genes encoding chloroplastic, mi- the Pol II transcription-initiation complex. A fourth class is tochondrial, peroxisomal, and cytosolic proteins are acti- architectural transcription factors that are also involved in vated. Similarly, a number of biotic and abiotic stresses remodeling DNA, e.g. by inducing bends that facilitate the cause a battery of genes to be activated as part of the binding of other proteins to the promoter. In this Update I will address how transcription factors regulate gene transcription in plants, as well as relying on 1 This work was supported by grants from the National Insti- tutes of Health and the U.S. Department of Agriculture. * Corresponding author; e-mail [email protected]; fax 1–310– Abbreviations: ABRC, ABA-responsive complex; ABRE, ABA- 206–3987. responsive element. 1111 1112 Singh Plant Physiol. Vol. 118, 1998 advances in other systems. The focus will be on activators Other forms of chromatin remodeling involving multi- and the importance of combinatorial control. First, I will protein complexes with ATP-dependent chromatin remod- comment on chromatin, chromatin remodeling, and the Pol eling activities have also been observed. A good example is II transcription-initiation complex, since it is the recruit- the SWI2/SNF2 complex, which was initially discovered ment and/or activity of the transcription-initiation com- through genetic studies as a transcriptional regulator of plex that is regulated by the gene-specific transcription specific genes in yeast (Stern et al., 1984; Neigeborn and factors, and this regulation occurs in the context of Carlson, 1984). A number of lines of evidence link the yeast chromatin. SWI2/SNF2 complex, which has a size of about 2,000,000 D, to chromatin remodeling (for review, see Cairns, 1998). Chromatin remodeling does not occur at promoters nor- mally regulated by the SWI2/SNF2 complex in strains with CHROMATIN REMODELING AND a defective SWI2/SNF2 complex. In addition, the purified TRANSCRIPTIONAL REGULATION SWI2/SNF2 complex was able to cause chromatin remod- Chromatin has several levels of structural organization, eling to occur in vitro. SWI2/SNF2-related complexes have with the basic unit being the nucleosome core, which con- also been identified in Drosophila melanogaster and humans. sists of 146 bp of DNA wrapped around a histone octamer. In D. melangoaster three additional chromatin-remodeling The presence of nucleosomes affects the accessibility of complexes have been identified, including NURF, which is DNA to other proteins, including transcription factors and able to stimulate the binding of a number of transcription the Pol II transcription-initiation complex. Higher orders of factors to chromatin templates (Tsukiyama and Wu, 1996). chromatin structure are also likely to affect transcription, The identification of distinct multiprotein complexes in- e.g. by leading to the organization of chromatin into active volved in chromatin remodeling raises important questions and silent regions. Exciting progress has been made re- regarding the role each plays in transcriptional regulation, cently on chromatin remodeling, including the involve- how they are targeted to specific promoters, and whether ment of histone acetylation/deacetylation on nucleosome they interact with other types of chromatin-remodeling conformation/stability, and the identification of novel pro- activities, such as histone acetylases. tein complexes that cause nucleosome disruption (for re- cent reviews, see Cairns, 1998; Struhl, 1998). THE POL II TRANSCRIPTION-INITIATION COMPLEX IS Histone acetylation was first reported in 1964 and at the A LARGE PROTEIN MACHINE time was proposed to play a role in the regulation of transcription (Allfrey et al., 1964). Studies during the next The Pol II transcription-initiation complex has a size in three decades supported this proposal, although until re- excess of 2,500,000 D (Fig. 1). Pol II itself is a complex cently the molecular mechanisms involved were not enzyme that in yeast consists of 14 subunits. Whereas Pol II known. Acetylation of histones occurs on Lys residues in catalyzes RNA synthesis, numerous other proteins are re- the amino-terminal tails that protrude from the surface of quired for promoter recognition and accurate transcription the nucleosome. Acetylation neutralizes the positive charge initiation. These include the six general transcription fac- of the histone tails and consequently causes a reduction in tors (Fig. 1), as well as a growing number of accessory their affinity for DNA. This leads to changes in nucleosome proteins. Some of these accessory proteins may serve as conformation and may lead to unfolding of the nucleo- coactivators or may be involved in chromatin remodeling, some. Thus, acetylation of histones is normally correlated whereas others probably provide regulatory functions that with transcriptional activity by facilitating the access of remain to be elucidated. Some of the general transcription transcription factors to the DNA, whereas deacetylation of factors are complex, e.g. TFIID is composed of TATA box histones is correlated with transcriptional repression. binding protein (TBP) and a number of TBP-associated A growing number of histone acetylases and histone factors (TAFs). deacetylases have been identified recently. Significantly, The general transcription factors and some of the acces- many of these proteins had
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